Chronic Mycobacterium marinum infection acts as a tumor promoter in Japanese Medaka (Oryzias latipes)

Comparative Biochemistry and Physiology - C Toxicology and Pharmacology

Volumn 149, Issue 2, 2009, Pages 152-160

  Broussard, Gregory W ^a   Norris, Michelle B ^b   Schwindt, Adam R ^c   Fournie, John W ^d   Winn, Richard N ^b   Kent, Michael L ^c   Ennis, Don G ^a  

^a UNIVERSITY OF LOUISIANA AT LAFAYETTE   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c OREGON STATE UNIVERSITY   (United States)

^d U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

Benzo a pyrene; Carcinogenesis; Hepatic neoplasia; Inflammation; Non tuberculosis mycobacteria; Oryzias latipes; Tuberculosis

Indexed keywords

BENZO[A]PYRENE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL INFECTION; CANCER MODEL; CANCER RISK; CARCINOGENESIS; CHRONIC DISEASE; DISEASE ASSOCIATION; FISH; HISTOLOGY; INFLAMMATION; LIVER ADENOMA; LIVER CELL CARCINOMA; MYCOBACTERIOSIS; MYCOBACTERIUM; MYCOBACTERIUM MARINUM; NEOPLASM; NONHUMAN; ORYZIAS; PRIORITY JOURNAL; TUBERCULOSIS; TUMOR PROMOTION;

CORYNEBACTERINEAE; MYCOBACTERIUM; MYCOBACTERIUM MARINUM; MYCOBACTERIUM TUBERCULOSIS; ORYZIAS LATIPES; ORYZIINAE;

EID: 64149123455     PISSN: 15320456     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpc.2008.09.011     Document Type: Article

References (77)

1. Abner S.R., Frazier C.L., Scheibe J.S., Krol R.A., Overstreet R.M., Walker W.W., and Hawkins W.E. Chronic inflammatory lesions in two small fish species, medaka (Oryzias latipes) and guppy (Poecilia reticulata), used in carcinogenesis bioassays. In: Stolen J.S., and Fletcher T.C. (Eds). Modulators of Fish Immune Responses: Models for Environmental Toxicology, Biomarkers, and Immunostimulators (1994), SOS Publications, Fair Haven, NJ, USA 219-233
2. Adams L.B., and Krahenbuhl J.L. Human leprosy. In: Boros D.L. (Ed). Granulomatous Infections and Inflammations: Cellular and Molecular Mechanisms (2003), ASM Press, Washington, DC 207-244
3. Alavanja M.C.R., Brownson R.C., Boice J.D., and Hock E. Preexisting lung disease and lung cancer among nonsmoking women. Am. J. Epidemiol. 136 (1992) 623-632
4. Ames B.N., Gold L.S., and Willett W.C. The causes and prevention of cancer. Proc. Natl. Acad. Sci. USA 92 (1995) 5258-5265
5. Arkush K.D., Mendoza L., Adkinson M.A., and Hedrick R.P. Observations on the life stages of Sphaerothecum destruens n. g., n. sp., a mesomycetozoean fish pathogen formally referred to as the rosette agent. J. Eukaryot. Microbiol. 50 (2003) 430-438
6. Aronson J.D. Spontaneous tuberculosis in saltwater fish. J. Infect. Dis. 39 (1926) 315-320
7. Astrofsky K.M., Schrenzel M.D., Bullis R.A., Smolowitz R.M., and Fox J.G. Diagnosis and management of atypical Mycobacterium spp. infections in established laboratory zebrafish (Brachydanio rerio) facilities. Comp. Med. 50 (2000) 666-672
8. Bailey W.S. Spirocerca-associated esophageal sarcomas. J. Am. Vet. Med. Assoc. 175 (1979) 148-150
9. Barker L.P., Porcella S.F., Wyatt R.G., and Small P.L.C. The Mycobacterium marinum G13 promoter is a strong sigma 70-like promoter that is expressed in Escherichia coli and mycobacteria species. FEMS Microbiol. Lett. 175 (1999) 79-85
10. Boorman G.A., Botts S., Bunton T.E., Fournie J.W., Harshbarger J.C., Hawkins W.E., Hinton D.E., Jokinen M.P., Okihiro M.S., and Wolfe M.J. Diagnostic criteria for degenerative, inflammatory, proliferative and neoplastic liver lesions in medaka (Oryzias latipes): consensus of a National Toxicology Program pathology working group. Toxicol. Pathol. 25 (1997) 202-210
11. Borm P.J.A., Knaapen A.M., Schins R.P.F., Godschalk R.W.L., and Van Schooten F.-J. Neutrophils amplify the formation of DNA adducts by benzo[a]pyrene in lung target cells. Environ. Health Perspect. 105 (1997) 1089-1093
12. Bowden G.T. Prevention of non-melanoma skin cancer by targeting ultraviolet-b-light signalling. Nat. Rev. Cancer 4 (2004) 23-35
13. Brenner A.V., Wang Z., Kleinerman R.A., Wang L., Zhang S., Metayer C., Chen K., Lei S., Cui H., and Lubin J.H. Previous pulmonary diseases and risk of lung cancer in Gansu Province, China. Int. J. Epidemiol. 30 (2001) 118-124
14. Broussard G.W., and Ennis D.G. Mycobacterium marinum produces long-term chronic infections in medaka: a new animal model for studying human tuberculosis. Comp. Biochem. Physiol. C 145 (2007) 45-54
15. Brown S.T., and Almenoff P.L. Pulmonary mycobacterial infections associated with neoplasia. Semin. Respir. Infect. 7 (1992) 104-113
16. Butler A.P., Trono D., Coletta L.D., Beard R., Fraijo R., Kazianis S., and Nairn R. Regulation of CDKN2A/B and Retinoblasoma genes in Xiphophorus melanoma. Comp. Biochem. Physiol. C 145 (2007) 145-155
17. Carr G.J., and Gorelick N.J. Statistical design and analysis of mutation studies in transgenic mice. Environ. Mol. Mutagen. 25 (1995) 246-255
18. Christen S., Hagen T.M., Shigenaga M.K., and Ames B.N. Chronic inflammation, mutation, and cancer. In: Parsonet J. (Ed). Microbes and malignancy: infection as a cause of human cancers (1999), Oxford Press, New York, NY 313-345
19. Cohen S.M. Infection, cell proliferation, and malignancy. In: Parsonet J. (Ed). icrobes and malignancy: infection as a cause of human cancers (1999), Oxford Press, New York, NY 313-345
20. Cope R.B., Stang B., Valentine B.A., and Bermudez L.E. Topical pre-exposure to cis-urocanic acid enhances Mycobacterium ulcerans infection in a Crl:IAF(HA)-hrBR hairless guinea pig model of Buruli ulcer disease. Photodermatol. Photoimmunol. Photomed. 20 (2004) 14-20
21. Domingo E.O., Warren K.S., and Stenger R.J. Increased incidence of hapatoma in mice with chronic schistosomiasis mansoni treated with a carcinogen. Am. J. Pathol. 51 (1967) 307-321
22. Ennis D.G. Mutagenesis. Encyclopedia of Life Sciences (2001), Scientific American/John Wiley and Sons, Ltd. 1-8 10.1038/npg.els.0000559 559
23. Evans M.R., Etuaful S.N., Amofah G., Adjei O., Lucas S., and Wansbrough-Jones M.H. Squamous cell carcinoma secondary to Buruli ulcer. Trans. R. Soc. Trop. Med. Hyg. 93 (1999) 63-64
24. Friedberg E.C., Walker G.C., and Siede W. DNA Repair and Mutagenesis (2006), ASM Press, Washington, D.C., USA
25. Gandhi N.R., Moll A., Sturm A.W., Pawinski R., Govender T., Lallo U., Zeller K., Andrews J., and Friendland G. Extensively drug-resistant tuberculosis as a cause of death in patients co-infected with tuberculosis and HIV in a rural area of South Africa. Lancet 368 (2006) 1575-1580
26. Gozlan R.E., St-Hilaire S., Feist S.W., Martin P., and Kent M.L. Disease threat to European fish. Nature 435 (2005) 1046
27. Grim K.C., Wolfe M., Hawkins W., Johnson R., and Wolf J. Intersex in Japanese medaka (Oryzias latipes) used as negative controls in toxicologic bioassays: a review of 54 cases from 41 studies. Environ. Toxicol. Chem. 26 (2007) 636-1643
28. Hashem M., and Boutros K. The influence of bilharzial infection on the carcinogenesis of the bladder. An experimental study. J. Egypt. Med. Assoc. 44 (1961) 598-606
29. Hawkins W.E., Walker W.W., and Overstreet R.M. Carcinogenicity tests using aquarium fish. In: Rand G.M. (Ed). Fundamentals of Aquatic Toxicology (1995), Taylor and Francis, New York, NY 225-263
30. Hawkins W.E., Walker W.W., Overstreet R.M., Lytle T.F., and Lytle J.S. Dose-related carcinogenic effects of water-borne benzo[a]pyrene on livers of two small fish species. Ecotoxicol. Environ. Saf. 16 (1998) 219-231
31. Hawkins W.W., Walker V.W., Fournie J.W., Manning C.S., and Krol R.M. Use of the Japanese medaka (Oryzias latipes) and guppy (Poecilia reticulata) in carcinogenesis testing under National Toxicology Program protocols. Toxicol. Pathol. 31 (2003) 88-91 (suppl.)
32. Hecht S.S. Tobacco carcinogens, their biomarkers and tobacco-induced cancer. Nat. Rev. Cancer 3 (2003) 733-744
33. Heckert R.A., Elankumaran S., Milani A., and Baya A. Detection of a new Mycobacterium species in wild striped bass in the Chesapeake Bay. J. Clin. Microbiol. 39 (2001) 710-715
34. Helleberg H., Xu H., Ehrengerg L., Hemminki K., Rannug U., and Törnqvist M. Studies of dose distribution, premutagenic events and mutation frequencies for benzo[a]pyrene aiming at low dose cancer risk estimation. Mutagenesis 16 (2001) 333-337
35. Hermon-Taylor J., Barnes N., Clark C., and Finlayson C. Mycobacterium paratuberculosis cervical lymphadenitis, followed by terminal ileitis similar to Crohn's Disease. Brit. Med. J. 316 (1998) 449-453
36. Hicks R.M., James C., and Webbe G. Effect of Schistosomiasis haematobium and N-butyl-N-(4-hydrooxybutyl)nitrosamine on the development of urothelial neoplasia in baboon. Br. J. Cancer 42 (1980) 730-755
37. Izzotti A., De Flora S., Cartiglia C., Are B.M., Longobardi M., Camoirano A., Mura I., Dore M.P., Scanu A.M., Rocca P.C., Maida A., and Pian A. Interplay between Helicobacter pylori and host gene polymorphisms in inducing oxidative DNA damage in the gastric mucosa. Carcinogenesis 28 (2007) 892-898
38. Kaattari I.M., Rhodes M.W., Kaattari S.L., and Shotts E.B. The evolving story of Mycobacterium tuberculosis clade members detected in fish. J. Fish Dis. 29 (2006) 509-520
39. Kasahara M., Naruse K., Sasaki S., et al. The medaka draft genome and insights into vertebrate genome evolution. Nature 447 (2007) 714-719
40. Kashiwada S., Goka K., Shiraishi H., Arizono K., Ozato K., Wakamatsu Y., and Hinton D.E. Age-dependent in situ hepatic and gill CYP1A activity in the see-through medaka (Oryzias latipes). Comp. Biochem. Physiol. C 145 (2007) 96-102
41. Kent M.L., Bishop-Stewart J.K., Matthews J.L., and Spitsbergen J.M. Pseudocapillaria tomentosa, a nematode pathogen of zebrafish (Danio rerio) kept in research colonies and associated neoplasms. Comp. Med. 52 (2002) 362-367
42. Kent M.L., Matthews J.L., Bishop-Stewart J.K., Whipps C.M., Watral V., Poort M., and Bermudez L. Mycobacteriosis in zebrafish (Danio rerio) research facilities. Comp. Biochem. Physiol. C 138 (2004) 383-390
43. Kim M.Y., and Wogan G.N. Mutagenesis of the supF gene of pSP189 replicating in AD293 cells cocultivated with activated macrophages: roles of nitric oxide and reactive oxygen species. Chem. Res. Toxicol. 19 (2006) 1483-1491
44. Kim I.-C., Kim Y.J., Yoon Y.-D., Kawamura S., Lee Y.-S., and Lee J.-S. Cloning of cytochrome P450 1A (CYP1A) genes from the hermaphrodite fish Rivulus marmoratus and the Japanese medaka Oryzias latipes. Mar. Environ. Res. 58 (2004) 125-129
45. Kusters J.G., van Vliet A.H.M., and Kuipers E.J. Pathogenesis of Helicobacter pylori infection. Clin. Microbiol. Rev. 19 (2006) 449-490
46. Lu H., Ouyang W., and Huang C. Inflammation, a key event in cancer development. Mol. Cancer Res. 4 (2006) 221-233
47. Morgenbesser S.D., Williams B.O., Jacks T., and Depinho R.A. p53-dependent apoptosis produced by Rb-deficiency in the developing mouse lens. Nature 371 (1994) 72-74
48. Morotona O.O., Martin H., Gentile G.J., and Gentile J.M. Enhanced liver cell mutations in trematode-infected Big Blue Mice. Mutat. Res. 484 (2001) 69-76
49. Mostafa M.H., Sheweita S.A., and O'Connor P.J. Relationship between schistosomiasis and bladder cancer. Clin. Microbiol. Rev. 12 (1999) 97-111
50. Ortutay C., Siermala M., and Vihinen M. Molecular characterization of the immune system: emergence of proteins, processes, and domains. Immunogenetics 59 (2007) 333-348
51. Ramsey F.L., and Schafer D.W. The Statistical Sleuth (1997), Wadsworth Publishing Company, Balmont, CA 742
52. Ranger B.S., Mahrous E.A., Mosi L., Adusumilli S., Lee R.E., Colorni A., Rhodes M., and Small P.L.C. Globally distributed mycobacterial fish pathogens produce a novel plasmid-encoded toxic macrolide, mycolactone F. Infect. Immun. 74 (2006) 6037-6045
53. Richardus J.H., and Smith T.C. Squamous cell carcinoma in chronic ulcers in leprosy: a review of 38 consecutive cases. Lepr. Rev. 62 (1991) 381-388
54. Rosin M., and Hofseth L.J. Schistosomiasis, bladder, and colon cancer. In: Parsonet J. (Ed). Microbes and malignancy: infection as a cause of human cancers (1999), Oxford Press, NY, New York 313-345
55. Rosin M.P., El Din Zaki S.S., Ward A.J., and Anwar W.A. Involvement of inflammatory reactions and elevated cell proliferation in the development of bladder cancer in schistosomiasis patients. Mutat. Res. 305 (1994) 283-292
56. Rosin M.P., Anwar W.A., and Ward A.J. Inflammation, chromosomal instability, and cancer: the schistosomiasis model. Cancer Res. 54 (1994) 1929s-1933s (suppl.)
57. Sanders G.E., and Swaim L.W. Atypical piscine mycobacteriosis in Japanese medaka (Oryzias latipes). Comp. Med. 51 (2001) 171-175
58. Shacter E., Beecham E.J., Covey J.M., Kohn K.W., and Potter M. Activated neutrophils induce prolonged DNA damage in neighboring cells. Carcinogenesis 9 (1988) 2297-2304
59. Shane B.S., de Boer J., Watson D.E., Haseman J.K., Glickman B.W., and Tindall K.R. LacI mutation spectra following benzo[a]pyrene treatment of Big Blue® mice. Carcinogenesis 21 (2000) 715-725
60. Swaim L.E., Connolly L.E., Volkman H.E., Humbert O., Born D.E., and Ramakrishnan L. Mycobacterium marinum infection of adult zebrafish causes caseating granulomatous tuberculosis and is moderated by adaptive immunity. Infect. Immun. 74 (2006) 6108-6117
61. Talaat A.M., Reimschuessel R., and Trucksis M. Identification of mycobacteria infecting fish to the species level using polymerase chain reaction and restriction enzyme analysis. Vet. Microbiol. 58 (1997) 229-237
62. Taniguchi Y., Takeda S., Furutani-Seiki M., Kamei Y., Todo T., Sasado T., Deguchi T., Kondoh H., Mudde J., Yamazoe M., Hidaka M., Mitani H., Toyoda A., Sakaki Y., Plasterk R.H.A., and Cuppen E. Generation of medaka gene knockout models by target-selected mutagenesis. Genome Biol. 7 (2006) R116
63. Teska J.D., Twerdok L.E., Beaman J., Curry M., and Finch R.A. Isolation of Mycobacterium abscessus from Japanese medaka. J. Aquat. Anim. Health 9 (1997) 234-238
64. Thamavit W., Tiwawech D., Moore M.A., Ito N., and Shirai T. Equivocal evidence of complete carcinogenicity after repeated infection of syrian hamsters with Opisthorchis viverrini. Toxicol. Pathol. 24 (1996) 493-497
65. Ucko M., Colorni A., Kvitt H., Diamant A., Zlotkin A., and Knibb W.R. Strain variation in Mycobacterium marinum fish isolates. Appl. Environ. Microbiol. 68 (2002) 5281-5287
66. Uemura N., Okamoto S., Yamamoto S., Matsumura N., Yamaguchi S., Yamakido M., Taniyama K., Sasaki N., and Schlemper R. Helicobacter pylori infection and the development of gastric cancer. N. Engl. J. Med. 345 (2001) 784-789
67. Van der Sar A.M., Appelmelk B.J., Vandenbroucke-Grauls C.M.J.E., and Bitter W. A star with stripes: zebrafish as an infection model. Trends Microbiol. 12 (2004) 451-457
68. Watral V., and Kent M.L. Pathogenesis of Mycobacterium spp. in zebrafish (Danio rerio) from research facilities. Comp. Biochem. Physiol. C 145 (2007) 55-60
69. Weitzman S.A., Weitberg A.B., Clark E.P., and Stossel T.P. Phagocytes as carcinogens: malignant transformation produced by human neutrophils. Science 227 (1985) 1231-1233
70. Winn R.N., and Norris M.B. Analysis of mutations in lambda transgenic medaka using the cll mutation assay. In: Ostrander G.K. (Ed). Techniques in aquatic toxicology. 2nd edition (2005), CRC Press, New York, NY 705-734
71. Winn R.N., Norris M.B., Brayer K.J., Torres C., and Muller S.L. Detection of mutations in transgenic fish carrying a bacteriophage lambda cll transgene target. Proc. Natl. Acad. Sci. USA 97 (2000) 12655-12660
72. Winn R.N., Kling H., and Norris M.B. Antimutagenicity of green tea polyphenols in the liver of transgenic medaka. Environ. Mol. Mutagen. 46 (2005) 88-95
73. Wu A.H., Fontham E.T.H., Reynolds P., Greenberg R.S., Buffler P., Liff J., Boyd P., Henderson B.E., and Correa P. Previous lung disease and risk of lung cancer among lifetime nonsmoking women in the United States. Am. J. Epidemiol. 141 (1995) 1023-1032
74. Yamashina K., Miller B.E., and Heppner G.H. Macrophage-mediated induction of drug resistant variants in a mouse mammary tumor cell line. Cancer Res. 46 (1986) 2396-2401
75. Zhenlin J., Wells M.C., Heater S.J., and Walter R.B. Multiple tissue gene expression analyses in Japanese medaka (Oryzias latipes) exposed to hypoxia. Comp. Biochem. Physiol. C 145 (2007) 134-144
76. Zhenlin J., Wells M.C., and Walter R.B. DNA microarray technology in toxicogenomics of aquatic models: methods and applications. Comp. Biochem. Physiol. C 145 (2007) 5-14
77. Zhuang J.C., Lin D., Lin C., Jethwaney D., and Wogan G.N. Genotoxicity associated with NO production in macrophages and co-cultured target cells. Free Radic. Biol. Med. 33 (2002) 94-102